Prelude. Cycle 1. Introduction. Cycle 2. Structure defines function. Cycle 3. Diversity of cortical functions is provided by inhibition. Cycle 4. Windows on the brain. Cycle 5. A system of rhythms: from simple to complex dynamics. Cycle 6. Synchronization by oscillation. Cycle 7. The brain's default state: self-organized oscillations in rest and sleep. Cycle 8. Perturbation of the default patterns by experience. Cycle 9. The gamma buzz: gluing by oscillations in the waking brain. Cycle 10. Perceptions and actions are brain state-dependent. Cycle 11. Oscillations in the "other cortex:" navigation in real and memory space. Cycle 12. Coupling of systems by oscillations. Cycle 13. The tough problem. References.

Rhythms of the brain

Interneurons of the hippocampus

Mammals adapt to a rapidly changing world because of the sophisticated cognitive functions that are supported by the neocortex. The neocortex, which forms almost 80% of the human brain, seems to have arisen from repeated duplication of a stereotypical microcircuit template with subtle specializations for different brain regions and species. The quest to unravel the blueprint of this template started more than a century ago and has revealed an immensely intricate design. The largest obstacle is the daunting variety of inhibitory interneurons that are found in the circuit. This review focuses on the organizing principles that govern the diversity of inhibitory interneurons and their circuits.

Interneurons of the neocortical inhibitory system.

In the cerebral cortex, diverse types of neurons form intricate circuits and cooperate in time for the processing and storage of information. Recent advances reveal a spatiotemporal division of labor in cortical circuits, as exemplified in the CA1 hippocampal area. In particular, distinct GABAergic (γ-aminobutyric acid–releasing) cell types subdivide the surface of pyramidal cells and act in discrete time windows, either on the same or on different subcellular compartments. They also interact with glutamatergic pyramidal cell inputs in a domain-specific manner and support synaptic temporal dynamics, network oscillations, selection of cell assemblies, and the implementation of brain states. The spatiotemporal specializations in cortical circuits reveal that cellular diversity and temporal dynamics coemerged during evolution, providing a basis for cognitive behavior.

/pdf/neuronal-diversity-and-temporal-dynamics-the-unity-of-16k3vh2yf1.pdf

Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations.

Slices of sensorimotor and anterior cingulate cortex from guinea pigs were maintained in vitro and bathed in a normal physiological medium. Electrophysiological properties of neurons were assessed with intracellular recording techniques. Some neurons were identified morphologically by intracellular injection of the fluorescent dye Lucifer yellow CH. Three distinct neuronal classes of electrophysiological behavior were observed; these were termed regular spiking, bursting, and fast spiking. The physiological properties of neurons from sensorimotor and anterior cingulate areas did not differ significantly. Regular-spiking cells were characterized by action potentials with a mean duration of 0.80 ms at one-half amplitude, a ratio of maximum rate of spike rise to maximum rate of fall of 4.12, and a prominent afterhyperpolarization following a train of spikes. The primary slope of initial spike frequency versus injected current intensity was 241 Hz/nA. During prolonged suprathreshold current pulses the frequency of firing adapted strongly. When local synaptic pathways were activated, all cells were transiently excited and then strongly inhibited. Bursting cells were distinguished by their ability to generate endogenous, all-or-none bursts of three to five action potentials. Their properties were otherwise very similar to regular-spiking cells. The ability to generate a burst was eliminated when the membrane was depolarized to near the firing threshold with tonic current. By contrast, hyperpolarization of regular-spiking (i.e., nonbursting) cells did not uncover latent bursting tendencies. The action potentials of fast-spiking cells were much briefer (mean of 0.32 ms) than those of the other cell types.(ABSTRACT TRUNCATED AT 250 WORDS)

Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex.

The coexistence of gamma-aminobutyric acid (GABA), glutamate decarboxylase (GAD), and cholecystokinin (CCK)- or somatostatin- immunoreactive material in the same neurons was studied in the hippocampus and visual cortex of the cat. One-micrometer-thick serial sections of the same neuron were reacted to reveal different antigens by the unlabeled antibody enzyme method. All CCK- and somatostatin- immunoreactive neurons in the cortex and all CCK-immunoreactive and the majority of somatostatin-immunoreactive neurons in the hippocampus that could be examined in serial sections were also immunoreactive for GABA. In neurons that were immunoreactive for GAD it was often possible to demonstrate immunoreactivity for one of the peptides as well as for GABA. GABA-immunoreactive neurons, as revealed by an antiserum to GABA, were present in all layers of the cortex and hippocampus, and their shape, size, and distribution were similar to GAD-immunoreactive neurons. All GAD-immunoreactive neurons were also positive for GABA, but the latter staining revealed additional neurons. CCK/GABA- and somatostatin/GABA-immunoreactive neurons were present mainly in layers II and upper III and in layers V and VI in the visual cortex. CCK/GABA- immunoreactive neurons were most frequently present in the strata oriens, pyramidale, and moleculare of the hippocampus and in the polymorph cell layer of the dentate gyrus. Somatostatin/GABA- immunoreactive neurons were localized mainly in the stratum oriens and in the hilus of the fascia dentata. The two peptides could not be found in the same neuron. The majority of neurons that were GABA immunoreactive did not stain for either peptide. The presence of CCK- and somatostatin-immunoreactive material in GABAergic cortical neurons raises the possibility that neuroactive peptides affect GABAergic neurotransmission.

https://www.jneurosci.org/content/jneuro/4/10/2590.full.pdf

Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin- immunoreactive material

Golgi-impregnated and gold-toned preparations of cat hippocampus were studied under the light and electron microscope in order to characterize synapses in contact with the axon initial segments of pyramidal neurons. The initial segment of the axon emits spine-like appendages and it was sometimes seen to be in apparent contact with thin varicose fibers that climbed along it. The latter type of varicose axon terminal segments occurred at the base of pyramidal neurons in all regions of the hippocampus and in the subiculum: they are 20 to 40 w long, contain 3 to 15 varicose swellings, and are interconnected by thin horizontal or arcadic fibers. It was established by electron microscopy of gold-toned material that light microscopically identified varicosities of these terminal segments were in symmetrical synaptic contact exclusively with axon initial segments; four of the initial segments in the CA1 region could be traced back to pyramidal neurons. Thus the pyramidal cell of the cat hippocampus receives input along its axon initial segment from boutons that probably originate from axoaxonic cells of the type found previously in the cerebral cortex and monkey hippocampus. Antiserum to glutamate decarboxylase was used to study the distribution and nature of cells and processes that bound the antiserum. Several different types of immunoreactive cell bodies were found in all layers in regions CA1 to CA3, suggesting that many kinds of GABAergic interneurons are present in the hippocampus. Fibers and varicosities that were immunoreactive for glutamate decarboxylase were also found in all layers. The most conspicuous patterns formed by immunoreactive varicosities were in the pyramidal cell layer, where they occurred as pericellular nets around all pyramidal neurons. Immunoreactive processes or varicosities also followed both apical and basal dendrites, but a very high density of immunoreactive varicosities was seen around fine (diameter 2 to 4 pm) tube-like structures that could sometimes be seen to lie at the base of pyramidal neurons. Electron microscopic analysis of immunoreactive structures that had first been identified in the light microscope established that the varicosities outlining such tube-like structures were boutons in symmetrical synaptic contact with the axon initial segments of pyramidal neurons; the other immunoreactive varicosities were boutons in symmetrical contact with cell bodies and apical and basal dendrites of pyramidal neurons. Detailed study of 19 axon initial segments showed that immunoreactive boutons occur most commonly along more distal parts of the initial segment, where they almost completely surround the axon and form symmetrical synapses not only along the main axon, but also with its spines. Since the glutamate decarboxylase-immunoreactive boutons comprised 92% of all symmetrical synaptic boutons along the initial segments, it was concluded that the axoaxonic cell uses y-aminobutyrate as its transmitter. It is suggested that the pyramidal neuron receives input from more than one type of GABAergic ’ We are grateful to Mrs. K. Boczko and Miss S. Thomas for excellent ’ To whom correspondence should be addressed. technical assistance. This work was supported by the Wellcome Trust, 3 Visiting Scientist from the Department of Neuroanatomy, Institute the Royal Society, the E. P. A. Cephalosporin Trust, the International of Higher Nervous Activity, Osaka University Medical School, 4-3-57 Cultural Institute (Budapest), the Japanese Society for the Promotion Nakanoshima, Kitaku, Osaka, Japan. Scholar of Herbert von Karajan of Sciences, the Hungarian Academy of Sciences, and Grants NS 13224 Neuroscience Research Trust. and EY 03909 from the National Institutes of Health.

https://www.jneurosci.org/content/jneuro/3/7/1450.full.pdf

Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons

A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells

The ultrastructural features and synaptic relationships of cholecystokinin (CCK) Immunoreactive cells of rat and cat hippocampus were studied using the unlabeled antibody immunoperoxidase technique and correlated light and electron microscopy. CCK-positive perikarya of variable shape and size were distributed in all layers and were particularly concentrated in stratum pyramidale and radiatum: the CCK-immunoreactive neurons were nonpyramidal in shape and the three most common types had the morphological features of tufted, bipolar, and multipolar cells.



Electron microscopic examination revealed that all the CCK-positive boutons established symmetrical (Gray's type II) synaptic contacts with perikarya and dendrites of pyramidal and nonpyramidal neurons. The origin of some of the boutons was established by tracing fine collaterals that arose from the main axon of two CCK-immunostained cells and terminated in the stratum pyramidale; these collaterals were then examined in the electron microscope. The axon of one such neuron exhibited a course parallel to the pyramidal layer and formed pericellular nets of synaptic boutons upon the perikarya of pyramidal neurons. This pattern of axonal arborization is very similar to that of some of the basket cells, previously suggested to be the anatomical correlate for pyramidal cell inhibition. Typical dendrites of pyramidal cells also received symmetrical synaptic contacts from CCK-immunoreactive boutons, and some of these boutons could be shown to originate from a local neuron in stratum radiatum. Many CCK-immunoreactive cells received CCK-labeled boutons upon their soma and dendritic shafts. Synaptic relationship, established by multiple Men passant boutons, was observed between CCK-positive interneurons of the stratum lacunosum-moleculare and radiatum. The soma and dendrites of the CCK-immunostained neurons also received symmetrical and asymmetrical synapses from nonimmuno-reactive boutons.



These results indicate that the CCK-immunoreactive neurons participate in complex local synaptic interactions in the hippocampus.

Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus.

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Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin- immunoreactive material

Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons

A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells

Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus.